Undisciplined thinking: morphology and Hennig’s unfinished revolution

Abstract

There was a time, not long ago and prior to Hennig (1966), when taxonomy was widely dismissed as a mere service to ‘real’– read experimental– sciences. Taxonomists were regarded by many to have nothing more to contribute to modern biology than the pragmatic role of identifying species and keeping track of their names. This was a legacy of the conflation of systematics with genetics by Huxley (1940), Mayr (1942) and others (see Wheeler, 1995, 2008a). Hennig re-elevated taxonomy, as phylogenetic systematics, to its rightful place as a rigorous, free-standing and central field of the biological sciences. Taxonomy is typically performed best when it is carried out for its own sake. Taxonomists are motivated to explore species, character diversity and phylogenetic relationships within monophyletic groups. The ultimate goal of taxonomists is a phylogenetic classification with associated scientific names, what Hennig described as biology’s general reference system. Oh yes, they make species identifiable, too. Current molecular initiatives, including DNA barcoding and DNA taxonomy, threaten to reduce species discovery as well as classifications to nothing more than a service. Because ‘new’ species would be ‘discovered’ on the basis of phenetic distances only, DNA barcoding might be described better as a disservice to biology (Prendini, 2005; Wheeler, 2005). After all, it offers only arbitrary averages, by contrast with explicitly testable alternatives, such as the phylogenetic species concept (Wheeler & Platnick, 2000). DNA taxonomy (in the sense of Tautz et al., 2003) is another flawed approach that would diminish the information content of classifications (e.g. Lipscomb et al., 2003). The trend in molecular phylogenetics (‘phylogenetic biology’) has been to increasingly marginalize the evidential basis of taxonomy and to treat the creation of ‘trees’ largely as a service to those same ‘real’ sciences. It is not coincidental that central to taxonomy ‘done for its own sake’ is a detailed study of characters, whereas most molecular phylogenies are published without characters. Morphology is regarded increasingly as an optional adjunct to molecular phylogeny, rather than an essential component of our understanding of species and their diversification. It is said that morphology provides few characters by comparison with molecular sources, and that its complex characters are inconveniently difficult to interpret and unacceptably subjective in their analysis. As a result, we are educating few young comparative morphologists and homogenizing ‘phylogenetic biology’ to be effectively little more than molecular ‘trees’ and morphology little more than literature reviews. The number of projects in which serious original morphological study is undertaken is alarmingly few, meaning that existing morphological hypotheses are untested, mistaken homology assessments are perpetuated and new morphological characters are undiscovered. The tragic loss represented by this neglect of comparative morphology has yet to be felt. Molecular phylogenies have concerned themselves largely with the reinterpretation of known taxa, and especially those bearing controversial ‘key’ morphological achievements, such as the evolution of flight in insects, vascular tissues in plants and, of course, the great tritomy of human, chimp and gorilla. Increasingly, it seems that molecular phylogenies are performed in service to others, to provide chronological patterns to biologists studying some attribute of organisms of sufficient complexity to be of inherent interest. The same putative virtue of simplicity that is claimed to make the interpretation of phylogeny from molecules less subjective deprives amino acids of sufficient complexity to store historical information. That only emerges from the next step in complexity: the sequence of amino acids in strands of DNA. Just as this minimal complexity adds some imperfect historical information, increasingly complex characters – genes, functionally linked genes, proteins, folding patterns, tissues, cells, ontogenetic pathways and morphology – each in turn potentially stores more and more historical information. This information is more difficult to interpret. Nevertheless, as has been well established, it can be made fully explicit and testable (Hennig, 1966; Farris, 1979; Gaffney, 1979; Nelson & Platnick, 1981; Wiley, 1981; Schuh, 2000). It takes time to begin to interpret the techniques used by Leonardo da Vinci to capture the mystique of Genevre D'Benci, and considerably less time to see the minimal technique behind Robert Rauschenberg’s White Painting. Are we to believe that it is not worth the investment of time in the case of the former to appreciate such content, or that all art should be monochromatic like the latter in order to make visits to art museums more time efficient? Could it be that it is complexity itself, including the seemingly endless variety in morphology, that draws us to study evolution and its history, and that having cladograms divorced from credible morphology and other characters is a vacuous endeavour, except as a service to others who do have ‘interesting’ character sets? Is it possible that there is a good reason that the same people who continue to visit zoos to marvel at giraffe necks, zebra stripes and rhinoceros horns would probably not make a trip to a public place to admire the percentage of differences between fragments of cytochrome oxidase subunit I genes amongst a comparable number of faceless samples? Molecular phylogenies have interest only by virtue of what they can tell us of the evolution of complex morphological characters, other characters or spatial distributions. The reality is that the external morphology of the vast majority of known species is described very incompletely, particularly in mega-diverse taxa such as insects. Moreover, the majority of characters and homology assumptions in groups such as insects are too infrequently tested to be considered to be corroborated. Furthermore, because an estimated 75% of all living species of insects remain unknown to science (Grimaldi & Engel, 2005), the morphology of the majority of species is entirely undocumented. Considering the imminent threats of extinction and the many species that are the last vestiges of nearly extinct clades, this would seem to be a particularly inopportune moment to abandon morphology. Those who advocate classifications that no longer require the preservation of whole specimens in collections (e.g. A. P. Vogler, personal communication), or allow species to be described only for which sequences are at least potentially available (Dayrat, 2005), are terribly misguided (Valdecasas et al., 2007) and ride on the tide of political correctness in support of all things molecular. This has all the intellectual depth of an advertisement for improved laundry detergent. Sadly, it sells. What we need in actuality is not DNA-exclusive or DNA-intensive classifications, but integrative taxonomy (e.g. Will et al., 2005). We need a taxonomy (a general reference system, a phylogenetic classification, including associated Linnaean names) that is informed by and summarizes as many sources of evidence as possible. Hennig (1966) referred to this as ‘holomorphology’. Combining excellent analyses of morphology, fossils, ontogeny and molecules will advance systematics much further than molecular phylogenies alone or in combination with superficial treatments of morphology or fossils or ontogeny. We need a taxonomy that integrates the expertise, diligence, knowledge, passion and talents of teams of specialists, each contributing something unique and excellent to collaborative studies of taxa. Considering that as many as three million insect species await discovery and that hundreds of thousands may not survive the present century, there would seem to be enough work for an army of full-time specialists of every stripe. If someone is a good collector and that is what he or she enjoys and excels at, then let us provide support for collecting; our collections are growing at an embarrassing rate in the midst of the biodiversity crisis, and we can afford to encourage and support as many collectors as can contribute to the effort. If someone is interested in comparative morphology, then let us support him or her to be the best morphologist he or she can be, and not require a dilution of good morphology by prescribed molecular laboratory work. If another is interested in molecular techniques, then let us sustain that interest, and so forth. There are valuable roles for specimen preparators, illustrators, phylogenetic analysts, palaeoentomologists, ontogeneticists, comparative ethologists, taxonomic cyberinfrastructure engineers, and on and on. Let us celebrate the diversity of interests and motivations that draw a diversity of people into systematic entomology, and not attempt to define what a good ‘systematist’ is so narrowly as to at once drive many talented contributors from the effort and homogenize and stifle the science to the point that it loses its most remarkable character: its innate ability to integrate many efforts towards a common goal and diverse sources of data into a reliable general reference system. The current fashion of multidisciplinary science is good in principle, but unfortunately has been implemented in such a way that taxonomy is expected to conform to assumptions and quantitative methods that are appropriate instead to experimental sciences. It seems to me that, in general, this is achieved more easily through transdisciplinary teams rather than multidisciplinary individuals. Into these teams the community of amateur taxonomists should be integrated, although their numbers appear also to be declining (Hopkins & Freckleton, 2002). Hennig’s (1966) concept of ‘holomorphology’ celebrated the long-established practice of taxonomy as a field capable of synthesizing evidence from all relevant comparative sources (e.g. Simpson, 1961). Hennig taught us that what matters is not the source of data, but rather how the data are analysed and whether special similarities are differentiated from raw overall similarity. The potent implications of Hennig’s theories have yet to be fully realized. Rather than welcoming the input of credible data from all sources, we have allowed technology and political correctness to drive the field towards one source of data and away from analytical methods that are consistent with Hennig’s theory of special similarity. Both are to the detriment of taxonomy. Real taxonomy is and has always been focused as much upon character analysis and evolution as upon the discovery of species and reconstruction of relationships. With the grand challenge questions of taxonomy unanswered (Cracraft, 2002; Page et al., 2005), we need to return to the core strengths of taxonomy, including explicit studies of characters. For the purpose of cladistic analysis, we simply need data that can and are analysed appropriately to reveal cladistic (as opposed to phenetic) patterns. In the context of cladistic analysis, molecules and morphology are just data, nothing more, nothing less. We need the best data we can have, and should not seek to homogenize the activities of those who gather it. Whether limited by talent, motivation, time or resources, many of us would prefer to focus on where our passions lie in order to make inspired contributions of the highest quality possible. For some of us, that means focusing exclusively on morphology or molecules or ontogeny or fossils. What matters is that as much data as possible are available; let us not confuse the need for taxonomy to have multiple data sources with an expectation that the full range is generated by each taxonomist. The discipline of taxonomy stands apart from the many fields of functional or general biology (Nelson & Platnick, 1981). It has taken centuries to refine the theoretical and epistemological justifications and assumptions of taxonomy; these advances should not be sacrificed on the altar of political correctness and modernity, in order to receive acceptance from experimental or molecular biologists. Students can be trained in a matter of months to sequence DNA proficiently and, if they generate large enough sums of external funding, can become celebrated as ‘good’ systematists. Morphologists must be educated over a period of years to work to high levels of excellence; they must master, in many cases, centuries of existing knowledge, a vast and technical vocabulary of terms required to discuss precisely complex characters and their component parts, understand intimately the theory behind concepts such as homology and synapomorphy as well as their use in a particular taxon, demonstrate a critical ‘eye’ capable of recognizing significant patterns of similarities or differences, learn to use alternative data sources as independent tests of sameness, and know how to collect, prepare, dissect and illustrate or image specific parts in a way that records and communicates complicated bits of visual knowledge. I do not suggest that there are not excellent molecular systematists that go far, far beyond the rote generation and analysis of data caricatured above; there are, and they deserve the same respect and support as good morphologists. The problem today, however, is not that they are denied stature and resources, it is that they alone receive them within systematic biology at the great detriment of the general reference system and growth of knowledge of morphology in particular. What is interesting at the heart of taxonomy is understanding the patterns of origin and diversification of complexity, not merely enumerating ‘species’ about which nothing is known concerning their structural uniqueness or relationships. Unless we support adequately the many facets of taxonomy, we impoverish our science to the point of undermining its importance. More importantly, unless we recognize that taxonomy is non-experimental (it cannot be commingled with, for example, ecology or population genetics) and that it is not subject to the same statistical tools appropriate to tokogenetic systems (Wheeler, 1995, 2004, 2008c), we necessarily diminish its unique contributions to biology. Combining experimental and historical sciences can only result in a kind of undisciplined thinking that ignores the epistemic of each The quality of taxonomy upon the of and respect for the differences between taxonomy and experimental biology. The diverse collectors to morphologists to molecular if as an in the advance of taxonomy without of the diversity and quality of I that we some teams with such diverse talents in of the that has been upon the field by an of the of molecular The that molecular data are ‘new’ is of Molecular sequences are the for the many morphological characters we have not yet The genes and morphological characters are, of precisely the same If the molecules do not the that into molecular what it is the This is that need only what we do and techniques were however, advances are place in used to and in comparative morphology. and image and a of other advances are If morphology can be with new has more information content and its hypotheses are subject to there would seem to be no for its has the the next generation of the very heart of the cyberinfrastructure are that support and new of are in an not of and like the but rather that work – and the This the for taxonomic when and specialists within and between taxa are linked to and all available knowledge of a (Wheeler, The have a for the of integrative taxonomy with science and et al., 2005; Wheeler, with such taxonomists would at last be to (Cracraft, 2002; Page et al., on an appropriately the of a cyberinfrastructure for taxonomy, we must the full range of of taxonomy from the molecular to the morphological and from the growth of collections to the of new The of teams and amongst museums is in the from the As as these projects are, they are limited by existing taxonomic The kind of and in the cyberinfrastructure would the and quality of such collaborative work et al., 2005; Wheeler, into a with that sequence a of and out species are, by and of taxonomy, not those motivated to a not understand a species in the context of its Students of can use to to without to learn the of in so they themselves of the they In a identifying species in of about most especially their morphology and can provide to but reduce taxonomy to a service rather than a or a serious The of these is the theoretical of DNA barcoding as it is (Prendini, 2005; Wheeler, 2005; & It can be a and new in our of species we have only in its we support taxonomists to and species that are by the use of DNA or we reduce species from testable hypotheses to arbitrary phenetic is a when divorced from theoretical If the of taxonomy is taxonomy will It is time to studies of morphology, new It not much or to the of molecular I challenge a few young about comparative morphology and to a as a new of morphologist to do and the by political with and engineers, who can tools morphologists can they contribute to teams focused on in our knowledge of species, phylogeny and Morphology is only if to understand the evolution of species on this We can our own as have There are many good to and support comparative morphology studies beyond characters available; I only a Morphology field biologists to plants and in the field without the need for characters are the only between and characters are the of The intellectual and associated with thinking about homology and are simply without In of of the who the only evidence that for species or monophyletic groups in an effort to make a point about the it is characters and their analysis that are at the heart of taxonomy. The work of morphology is far from It is to that our knowledge of morphology and is for all species, for most species and for the majority of living species that are unknown to The of of morphological for most insects is Moreover, it that every homology is an in need of critical as are about the of characters amongst species (Nelson & Platnick, 1981). 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